Isolation of Anti-Inflammatory and Epithelium Reinforcing <i>Bacteroides</i> and <i>Parabacteroides</i> Spp. from A Healthy Fecal Donor

Altered intestinal microbiota is associated with systemic and intestinal diseases, such as inflammatory bowel disease (IBD). Dysbiotic microbiota with enhanced proinflammatory capacity is characterized by depletion of anaerobic commensals, increased proportion of facultatively anaerobic bacteria, as...

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Main Authors: Kaisa Hiippala, Veera Kainulainen, Maiju Suutarinen, Tuomas Heini, Jolene R. Bowers, Daniel Jasso-Selles, Darrin Lemmer, Michael Valentine, Riley Barnes, David M. Engelthaler, Reetta Satokari
Format: Article
Language:English
Published: MDPI AG 2020-03-01
Series:Nutrients
Subjects:
LPS
Online Access:https://www.mdpi.com/2072-6643/12/4/935
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spelling doaj-0e3cb4e4b6c344379c742c279af36e072020-11-25T02:28:44ZengMDPI AGNutrients2072-66432020-03-011293593510.3390/nu12040935Isolation of Anti-Inflammatory and Epithelium Reinforcing <i>Bacteroides</i> and <i>Parabacteroides</i> Spp. from A Healthy Fecal DonorKaisa Hiippala0Veera Kainulainen1Maiju Suutarinen2Tuomas Heini3Jolene R. Bowers4Daniel Jasso-Selles5Darrin Lemmer6Michael Valentine7Riley Barnes8David M. Engelthaler9Reetta Satokari10Human Microbiome Research Program, Faculty of Medicine, University of Helsinki, 00290 Helsinki, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, 00290 Helsinki, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, 00290 Helsinki, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, 00290 Helsinki, FinlandTranslational Genomics Research Institute, Pathogen and Microbiome Division, Flagstaff, AZ 86001, USATranslational Genomics Research Institute, Pathogen and Microbiome Division, Flagstaff, AZ 86001, USATranslational Genomics Research Institute, Pathogen and Microbiome Division, Flagstaff, AZ 86001, USATranslational Genomics Research Institute, Pathogen and Microbiome Division, Flagstaff, AZ 86001, USATranslational Genomics Research Institute, Pathogen and Microbiome Division, Flagstaff, AZ 86001, USATranslational Genomics Research Institute, Pathogen and Microbiome Division, Flagstaff, AZ 86001, USAHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, 00290 Helsinki, FinlandAltered intestinal microbiota is associated with systemic and intestinal diseases, such as inflammatory bowel disease (IBD). Dysbiotic microbiota with enhanced proinflammatory capacity is characterized by depletion of anaerobic commensals, increased proportion of facultatively anaerobic bacteria, as well as reduced diversity and stability. In this study, we developed a high-throughput in vitro screening assay to isolate intestinal commensal bacteria with anti-inflammatory capacity from a healthy fecal microbiota transplantation donor. Freshly isolated gut bacteria were screened for their capacity to attenuate <i>Escherichia coli</i> lipopolysaccharide (LPS)-induced interleukin 8 (IL-8) release from HT-29 cells. The screen yielded a number of <i>Bacteroides</i> and <i>Parabacteroides</i> isolates, which were identified as <i>P. distasonis</i>, <i>B. caccae</i>, <i>B. intestinalis</i>, <i>B. uniformis</i>, <i>B. fragilis</i>, <i>B. vulgatus</i> and <i>B. ovatus</i> using whole genome sequencing. We observed that a cell-cell contact with the epithelium was not necessary to alleviate in vitro inflammation as spent culture media from the isolates were also effective and the anti-inflammatory action did not correlate with the enterocyte adherence capacity of the isolates. The anti-inflammatory isolates also exerted enterocyte monolayer reinforcing action and lacked essential genes to synthetize hexa-acylated, proinflammatory lipid A, part of LPS. Yet, the anti-inflammatory effector molecules remain to be identified. The <i>Bacteroides</i> strains isolated and characterized in this study have potential to be used as so-called next-generation probiotics.https://www.mdpi.com/2072-6643/12/4/935bacteroidesgut homeostasishost-microbe interactionsimmunomodulationLPSnext-generation probiotics
collection DOAJ
language English
format Article
sources DOAJ
author Kaisa Hiippala
Veera Kainulainen
Maiju Suutarinen
Tuomas Heini
Jolene R. Bowers
Daniel Jasso-Selles
Darrin Lemmer
Michael Valentine
Riley Barnes
David M. Engelthaler
Reetta Satokari
spellingShingle Kaisa Hiippala
Veera Kainulainen
Maiju Suutarinen
Tuomas Heini
Jolene R. Bowers
Daniel Jasso-Selles
Darrin Lemmer
Michael Valentine
Riley Barnes
David M. Engelthaler
Reetta Satokari
Isolation of Anti-Inflammatory and Epithelium Reinforcing <i>Bacteroides</i> and <i>Parabacteroides</i> Spp. from A Healthy Fecal Donor
Nutrients
bacteroides
gut homeostasis
host-microbe interactions
immunomodulation
LPS
next-generation probiotics
author_facet Kaisa Hiippala
Veera Kainulainen
Maiju Suutarinen
Tuomas Heini
Jolene R. Bowers
Daniel Jasso-Selles
Darrin Lemmer
Michael Valentine
Riley Barnes
David M. Engelthaler
Reetta Satokari
author_sort Kaisa Hiippala
title Isolation of Anti-Inflammatory and Epithelium Reinforcing <i>Bacteroides</i> and <i>Parabacteroides</i> Spp. from A Healthy Fecal Donor
title_short Isolation of Anti-Inflammatory and Epithelium Reinforcing <i>Bacteroides</i> and <i>Parabacteroides</i> Spp. from A Healthy Fecal Donor
title_full Isolation of Anti-Inflammatory and Epithelium Reinforcing <i>Bacteroides</i> and <i>Parabacteroides</i> Spp. from A Healthy Fecal Donor
title_fullStr Isolation of Anti-Inflammatory and Epithelium Reinforcing <i>Bacteroides</i> and <i>Parabacteroides</i> Spp. from A Healthy Fecal Donor
title_full_unstemmed Isolation of Anti-Inflammatory and Epithelium Reinforcing <i>Bacteroides</i> and <i>Parabacteroides</i> Spp. from A Healthy Fecal Donor
title_sort isolation of anti-inflammatory and epithelium reinforcing <i>bacteroides</i> and <i>parabacteroides</i> spp. from a healthy fecal donor
publisher MDPI AG
series Nutrients
issn 2072-6643
publishDate 2020-03-01
description Altered intestinal microbiota is associated with systemic and intestinal diseases, such as inflammatory bowel disease (IBD). Dysbiotic microbiota with enhanced proinflammatory capacity is characterized by depletion of anaerobic commensals, increased proportion of facultatively anaerobic bacteria, as well as reduced diversity and stability. In this study, we developed a high-throughput in vitro screening assay to isolate intestinal commensal bacteria with anti-inflammatory capacity from a healthy fecal microbiota transplantation donor. Freshly isolated gut bacteria were screened for their capacity to attenuate <i>Escherichia coli</i> lipopolysaccharide (LPS)-induced interleukin 8 (IL-8) release from HT-29 cells. The screen yielded a number of <i>Bacteroides</i> and <i>Parabacteroides</i> isolates, which were identified as <i>P. distasonis</i>, <i>B. caccae</i>, <i>B. intestinalis</i>, <i>B. uniformis</i>, <i>B. fragilis</i>, <i>B. vulgatus</i> and <i>B. ovatus</i> using whole genome sequencing. We observed that a cell-cell contact with the epithelium was not necessary to alleviate in vitro inflammation as spent culture media from the isolates were also effective and the anti-inflammatory action did not correlate with the enterocyte adherence capacity of the isolates. The anti-inflammatory isolates also exerted enterocyte monolayer reinforcing action and lacked essential genes to synthetize hexa-acylated, proinflammatory lipid A, part of LPS. Yet, the anti-inflammatory effector molecules remain to be identified. The <i>Bacteroides</i> strains isolated and characterized in this study have potential to be used as so-called next-generation probiotics.
topic bacteroides
gut homeostasis
host-microbe interactions
immunomodulation
LPS
next-generation probiotics
url https://www.mdpi.com/2072-6643/12/4/935
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